Search

Insensitive munitions compounds (IMCs) are emerging nitroaromatic contaminants developed by the military as safer-to-handle alternatives to conventional explosives. Biotransformation of nitroaromatics via microbial respiration has only been reported for a limited number of substrates. Important soil microorganisms can respire natural organic matter (NOM) by reducing its quinone moieties to hydroquinones. Thus, we investigated the NOM respiration combined with the abiotic reduction of nitroaromatics by the hydroquinones formed. First, we established nitroaromatic concentration ranges that were nontoxic to the quinone respiration. Then, an enrichment culture dominated by Geobacter anodireducens could indirectly reduce a broad array of nitroaromatics by first respiring NOM components or the NOM surrogate anthraquinone-2,6-disulfonate (AQDS). Without quinones, no nitroaromatic tested was reduced except for the IMC 3-nitro-1,2,4-triazol-5-one (NTO). Thus, the quinone respiration expanded the spectrum of nitroaromatics susceptible to transformation. The system functioned with very low quinone concentrations because NOM was recycled by the nitroaromatic reduction. A metatranscriptomic analysis demonstrated that the microorganisms obtained energy from quinone or NTO reduction since respiratory genes were upregulated when AQDS or NTO was the electron acceptor. The results indicated microbial NOM respiration sustained by the nitroaromatic-dependent cycling of quinones. This process can be applied as a nitroaromatic remediation strategy, provided that a quinone pool is available for microorganisms.

Metagenomic surveys have revealed that natural microbial communities are predominantly composed of sequence-discrete, species-like populations but the genetic and/or ecological processes that maintain such populations remain speculative, limiting our understanding of population speciation and adaptation to perturbations. To address this knowledge gap, we sequenced 112 Salinibacter ruber isolates and 12 companion metagenomes from four adjacent saltern ponds in Mallorca, Spain that were experimentally manipulated to dramatically alter salinity and light intensity, the two major drivers of this ecosystem. Our analyses showed that the pangenome of the local Sal. ruber population is open and similar in size (~15,000 genes) to that of randomly sampled Escherichia coli genomes. While most of the accessory (noncore) genes were isolate-specific and showed low in situ abundances based on the metagenomes compared to the core genes, indicating that they were functionally unimportant and/or transient, 3.5% of them became abundant when salinity (but not light) conditions changed and encoded for functions related to osmoregulation. Nonetheless, the ecological advantage of these genes, while significant, was apparently not strong enough to purge diversity within the population. Collectively, our results provide an explanation for how this immense intrapopulation gene diversity is maintained, which has implications for the prokaryotic species concept.

Microbial communities thriving in hypersaline brines of solar salterns are highly resistant and resilient to environmental changes, and salinity is a major factor that deterministically influences community structure. Here, we demonstrate that this resilience occurs even after rapid osmotic shocks caused by a threefold change in salinity (a reduction from 34 to 12% salts) leading to massive amounts of archaeal cell lysis. Specifically, our temporal metagenomic datasets identified two co-occurring ecotypes within the most dominant archaeal population of the brines Haloquadratum walsbyi that exhibited different salt concentration preferences. The dominant ecotype was generally more abundant and occurred in high-salt conditions (34%); the low abundance ecotype always co-occurred but was enriched at salinities around 20% or lower and carried unique gene content related to solute transport and gene regulation. Despite their apparent distinct ecological preferences, the ecotypes did not outcompete each other presumably due to weak functional differentiation between them. Further, the osmotic shock selected for a temporal increase in taxonomic and functional diversity at both the Hqr. walsbyi population and whole-community levels supporting the specialization-disturbance hypothesis, that is, the expectation that disturbance favors generalists. Altogether, our results provide new insights into how intraspecies diversity is maintained in light of substantial gene-content differences and major environmental perturbations.

Microbial communities thriving in hypersaline brines of solar salterns are highly resistant and resilient to environmental changes, and salinity is a major factor that deterministically influences community structure. Here, we demonstrate that this resilience occurs even after rapid osmotic shocks caused by a threefold change in salinity (a reduction from 34 to 12% salts) leading to massive amounts of archaeal cell lysis. Specifically, our temporal metagenomic datasets identified two co-occurring ecotypes within the most dominant archaeal population of the brines Haloquadratum walsbyi that exhibited different salt concentration preferences. The dominant ecotype was generally more abundant and occurred in high-salt conditions (34%); the low abundance ecotype always co-occurred but was enriched at salinities around 20% or lower and carried unique gene content related to solute transport and gene regulation. Despite their apparent distinct ecological preferences, the ecotypes did not outcompete each other presumably due to weak functional differentiation between them. Further, the osmotic shock selected for a temporal increase in taxonomic and functional diversity at both the Hqr. walsbyi population and whole-community levels supporting the specialization-disturbance hypothesis, that is, the expectation that disturbance favors generalists. Altogether, our results provide new insights into how intraspecies diversity is maintained in light of substantial gene-content differences and major environmental perturbations.

Microbial communities thriving in hypersaline brines of solar salterns are highly resistant and resilient to environmental changes, and salinity is a major factor that deterministically influences community structure. Here, we demonstrate that this resilience occurs even after rapid osmotic shocks caused by a threefold change in salinity (a reduction from 34 to 12% salts) leading to massive amounts of archaeal cell lysis. Specifically, our temporal metagenomic datasets identified two co-occurring ecotypes within the most dominant archaeal population of the brines Haloquadratum walsbyi that exhibited different salt concentration preferences. The dominant ecotype was generally more abundant and occurred in high-salt conditions (34%); the low abundance ecotype always co-occurred but was enriched at salinities around 20% or lower and carried unique gene content related to solute transport and gene regulation. Despite their apparent distinct ecological preferences, the ecotypes did not outcompete each other presumably due to weak functional differentiation between them. Further, the osmotic shock selected for a temporal increase in taxonomic and functional diversity at both the Hqr. walsbyi population and whole-community levels supporting the specialization-disturbance hypothesis, that is, the expectation that disturbance favors generalists. Altogether, our results provide new insights into how intraspecies diversity is maintained in light of substantial gene-content differences and major environmental perturbations.

While the dynamics of microbial community assembly driven by environmental perturbations have been extensively studied, our understanding is far from complete, particularly for light‐induced perturbations. Extremely halophilic communities thriving in coastal solar salterns are mainly influenced by two environmental factors—salt concentrations and high sunlight irradiation. By experimentally manipulating light intensity through the application of shading, we showed that light acts as a deterministic factor that ultimately drives the establishment of recurrent microbial communities under near‐saturation salt concentrations. In particular, the stable and highly change‐resistant communities that established under high‐light intensities were dominated (>90% of metagenomic reads) by Haloquadratum spp. and Salinibacter spp. On the other hand, under 37‐fold lower light intensity, different, less stable and change‐resistant communities were established, mainly dominated by yet unclassified haloarchaea and relatively diverse photosynthetic microorganisms. These communities harboured, in general, much lower carotenoid pigment content than their high‐irradiation counterparts. Both assemblage types appeared to be highly resilient, re‐establishing when favourable conditions returned after perturbation (i.e. high‐irradiation for the former communities and low‐irradiation for the latter ones). Overall, our results revealed that stochastic processes were of limited significance to explain these patterns.

Modeling crude-oil biodegradation in sediments remains a challenge due in part to the lack of appropriate model organisms. Here we report the metagenome-guided isolation of a novel organism that represents a phylogenetically narrow (>97% 16S rRNA gene identity) group of previously uncharacterized, crude-oil degraders. Analysis of available sequence data showed that these organisms are highly abundant in oiled sediments of coastal marine ecosystems across the world, often comprising ~30% of the total community, and virtually absent in pristine sediments or seawater. The isolate genome encodes functional nitrogen fixation and hydrocarbon degradation genes together with putative genes for biosurfactant production that apparently facilitate growth in the typically nitrogen-limited, oiled environment. Comparisons to available genomes revealed that this isolate represents a novel genus within the Gammaproteobacteria, for which we propose the provisional name “Candidatus Macondimonas diazotrophica” gen. nov., sp. nov. “Ca. M. diazotrophica” appears to play a key ecological role in the response to oil spills around the globe and could be a promising model organism for studying ecophysiological responses to oil spills.

While the dynamics of microbial community assembly driven by environmental perturbations have been extensively studied, our understanding is far from complete, particularly for light-induced perturbations. Extremely halophilic communities thriving in coastal solar salterns are mainly influenced by two environmental factors—salt concentrations and high sunlight irradiation. By experimentally manipulating light intensity through the application of shading, we showed that light acts as a deterministic factor that ultimately drives the establishment of recurrent microbial communities under near-saturation salt concentrations. In particular, the stable and highly change-resistant communities that established under high-light intensities were dominated (>90% of metagenomic reads) by Haloquadratum spp. and Salinibacter spp. On the other hand, under 37-fold lower light intensity, different, less stable and change-resistant communities were established, mainly dominated by yet unclassified haloarchaea and relatively diverse photosynthetic microorganisms. These communities harboured, in general, much lower carotenoid pigment content than their high-irradiation counterparts. Both assemblage types appeared to be highly resilient, re-establishing when favourable conditions returned after perturbation (i.e. high-irradiation for the former communities and low-irradiation for the latter ones). Overall, our results revealed that stochastic processes were of limited significance to explain these patterns.